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Food Selection and Internal Processing in Archegozetes Longisetosus (Acari: Oribatida)

Posted on: Saturday, 8 May 2004, 06:00 CDT

KEYWORDS Oribatlda; Nutritional biology; Food selection; Algae; Fungi; Paper; Starvation

Summary

The nutritional biology of the oribatid mite Archeqozetes longisetosus Aoki was examined using a control (starvation) and four types of food: Protococcus sp. algae from tree bark, two fungi- Stachybothrys sp. and Alternaria sp. and filter paper. Direct observations, histology, enzymology and plating techniques were employed to record contact with food, contents and structure of the alimentary tract, presence and viability of bacterial microorganisms inside the mite body, and chitinase and cellulase activity of mite homogenates. Algae were highly palatable, resulting in high apocrine secretion and guts that were continuously full. Initially there was no evidence of chitinase or cellulase production. Chitinase activity started after 10 days, probably due to consumption of fungi that invaded the algal cover, and correlated with the presence of chitinolytic bacteria (Serratia rubidea) in the mite homogenate. Alternaria was grazed intensively, but cell walls of spores and hyphae remained intact and no chitinase was detected suggesting that only cell contents were enzymatically digested. Stachybothrys sp. was rejected as food. The bacterium Alcaligenes faecalis was dominant in homogenates in each of the treatments, but under starvation Achromobacter xylosoxidans became co-dominant. Cellulase activity was not detected in any treatment, but strong chitinase activity was induced with a filter paper (colonized by invasive fungi) diet. Furthermore, bacteria were common in mesenchyme between the internal organs in the filter paper and starvation treatments.

2004 Elsevier GmbH. All rights reserved.

Introduction

Many oribatid mites-in the traditional sense of the group (without Astigmata)-are associated with decomposition processes in the soil system, where they ingest mainly particles of dead higher plant structural material and fungi. Specialists exist, but many species consume a wide range of food. Some species exhibit wide zoogeographical distribution and, if the literature is an accurate indication, their nutritional biology can also vary with location.

Such knowledge comes largely from investigation of food in the gut of field-collected animals that have been dissected or cleared in lactic acid, or from cafeteria-style experiments (e.g. Schuster, 1956; Hartenstein, 1962; Czajkowska, 1970; Behan and Hill, 1978; Pankiewicz-Nowicka et al., 1984). Less commonly, digestive enzyme activity has been recorded from whole-body homogenates (e.g. Luxton, 1972; Dinsdale, 1974; Siepel and de Ruiter-Dijkman, 1993), but this has typically been done without precise knowledge of mite diet before homogenization, or of their current gut microflora. The latter can vary according to the age and diet of the mite, and are suspected to secrete some of the detected enzymes (Stefaniak and Seniczak, 1981; Wolf and Rockett, 1984).

However, much remains to be learned before we understand the nutritional potential of any oribatid mite species, or the reasons for temporal or site variation in what they eat. Details of internal processes, such as enzyme production, actual digestion inside the gut, assimilation of nutrients, and internal microbial communities, must be placed in an environmental context. For example, Smrz and Catska (1989) found that the soil-dwelling astigmatic mite Tymphagus putrescentiae consumes and assimilates fungi differently, in ways that seem to relate to environmental conditions and the nutritional value of the particular fungus. Thus, a combination of internal and external factors appears to be important in understanding nutritional biology (Smrz, 2002a, b).

In this study, we use such an approach to compare the affinity for and utilization of various foods offered to the oribatid mite, Archegozetes longisetosus Aoki (Malaconothroidea: Trhypochthoniidae) in a laboratory setting.

Materials and methods

Choice of experimental species

Archegozetes longisetosus is an oribatid mite with a pan- tropical distribution (Aoki, 1965; Beck, 1967; Palmer and Norton, 1991). Due to its relatively large size, short generation time, high fecundity and ease of culture it is becoming the oribatid mite most studied under laboratory conditions. In addition to investigations of life cycle (Honciuc, 1996; Estrada-Venegas et al., 1999) it has been a subject of heavy-metal toxicology (Seniczak and Seniczak, 1998, 2002), embryology (Thomas and Telford, 1999) and developmental genetics (Telford and Thomas, 1998a, b). Detailed work on the ultrastructure of its alimentary tract and mouthparts is also underway (G. Alberti and A. Seniczak, pers. comm., 2003). Like all members of its superfamily, A. iongisetosus reproduces only by female parthenogenesis (thelyutoky) and available evidence suggests that the offsprings may be genetic clones of their mother (Palmer and Norton, 1992). Thus, investigators can rear large numbers of descendants from a single female, in order to study the biological effects of natural environmental variations or perturbations (e.g. Seniczak, 1998). Some preliminary information on feeding biology exists (see Discussion) and since all stages are translucent, the formation and characteristics of food boli or fecal pellets are easily observed.

Origin of specimens

Specimens used in this study originated from a culture started by R.A. Norton in 1993. The original mites were from a Tullgren-funnel extraction of decomposing coconut debris obtained on 1 April 1993 at Luquillo, Puerto Rico. Late in 1993 the culture was reduced to a single female, from which all subsequent mites have descended. In the Charles University laboratory, these mites have been cultured on the green alga Protococcus sp., which grows naturally on the bark of local apple trees.

Experimental design

The experiment was performed at room temperature (20-22C) in closed glass rearing jars (220 cm^sup 3^) with substrates of a plaster-of-Paris/charcoal mixture that was moistened at 3-day intervals with 10ml of water. The experiment was started with 100 tritonymphs of A. longiseiosus per jar, with each jar assigned one of five nutritional regimes: (1) Protococcus sp. algae, from the same source used in culture; (2) the fungus Stachybothrys sp., cultured on filter paper; (3) the fungus Alternaria sp., cultured on malt agar (pH 6.8); (4) filter paper; and (5) no food provided (starvation). Both fungi originated from the fungal collection at Charles University and were introduced into the experimental jars on 3 3 cm fragments of their growth medium. Filter paper or alga- covered bark was introduced as similar-sized fragments, in the respective treatments. No offered food was directly noxious or toxic to the mites. The treatments were triplicated, and allowed to run for 10 days. Samples of specimens were removed for histology and homogenization after intervals of 1, 3, 7 and 10 days.

In the previous work on mites (Smrz, 1996, 1998, 2002a, b), direct microanatomical responses to feeding regime have been observed after similarly short experiments, however, this time frame is too short to measure other ecological parameters (population changes, adult/juvenile ratio).

Observations and data collection

Mites were intermittently observed throughout the experiment, with searching behavior and persistence (time spent on the food) being specifically noted as indicators of food affinity. Activity in the food pathway was investigated both histologically and enzymologically. Specimens (10 tritonymphs per jar per treatment at each sampling time) used in histology were fixed in Bouin-Dubosque- Brasil fluid, as modified for mites by Smrz (1989), embedded in Histoplast (Serva), sectioned by MSE microtome (thickness 3000-5000 nm), and stained by Masson's trichrome. The sections were observed with a Provis AX 70 microscope (Olympus) equipped with Nomarski DIC optics and analyzed in the Microimage 3.0 image analysis program (Olympus). Records were kept on the microanatomy of the alimentary tract walls, secretory activity of mesenteron and mesenteral caeca, the nature of food boli, and the presence of microorganisms in the mesenchymal tissue between the internal organs.

At the stated intervals, 10 additional mites were selected from each treatment jar, pooled, and homogenized (see Smrz et al., 1991; Smrz, 2000). Homogenates were tested for the activity of enzymes that act on the major components of fungal and plant cell wall- chitinase and cellulase, respectively-using the method of Smrz (2000). This method is based on digestion by the homogenate of a thin layer of cellulose or carboxymethylchitin. Internal microorganisms were simultaneously plated from the homogenates (Smrz et al., 1991), and specialists at the Czech Collection of Microorganisms (CCM), Brno (Czech Republic), an internationally certified laboratory, identified the isolated bacteria.

Results

There was little variation between mites within treatments. Experimental results are described below, grouped according to nutritional regime and are further summarized in Table 1.

Protococcus sp.

All mites encountered the bark during the first 2 h, and then remained there. Initially, they stayed on the algal cover, but as this was consumed, mites progressively spread over the entire bark surface, including the underside. After 7 days most algae had been consumed,and mites were often found on the accumulating excrements on the bottom of the jar, underneath the bark. Fecal boli were green while inside the mite body, but darkened to black about a week after defecation.

At each sampling time, all parts of the alimentary tract contained food boli. Algal cells dominated the boli at days 1 and 3 (Fig. 1a). After this time, the tract contained an increasing proportion of fungal spores and hyphae (compare Fig. 1b). The mesenteral caeca exhibited substantial secretory activity for the full length of the experiment, as indicated by enzyme granules that filled their translucent cells and the presence of more than 10 proliferated cell apices per histological section. By day 3, however, very darkly stained, vacuolized cells appeared in the caecal walls. Apocrine secretion became more intensive in the transparent cells adjoining these dark ones. Sparse bacterial cells occurred in mesenchymal tissue between the internal organs, and Alcaligenes faecalis was the dominant bacterium inside the mite body, as determined by the plating of homogenate; few other bacteria formed colonies on plates. Neither chitinase nor cellulase activity was detected in the whole body homogenate during the first week.

Between 7 and 10 days, the proportion of fungal propagules increased in food boli and apocrine secretion was very intensive. The bacterium Serratia rubidaea was plated from the homogenate as one of the dominant species (together with Alcaligenes faecalis). Minimal chitinase activity was detected in the homogenate as well.

Stachybothrys sp.

Mites avoided the dense fungal cover and instead walked on the plaster substrate. They irregularly visited the margin of the filter paper fragment bearing the fungus, but were more frequently observed on the accumulating mite feces.

The alimentary tract contained food boli only sporadically, and not in all parts. Boli were formed by mucus, various small particles, and rare fragments of paper (Figs. 1c and d). After 7 days, food boli in the mesenteron became compact and coated by a mucoid layer. These boli contained several types of particles, including fungal propagules and spores (Fig. 2a), but the fungal elements were not from Stachybothrys. Paper fragments were not identifiable in these compact boli or in feces.

Table 1. Microanatomical, microbiological and enzymatic responses of Archegozetes longisetosus to offered food in experiment

Secretory activity was lower, and the mesenteral and caecal walls were thinner, than in mites fed with algae. No bacterial groups were observed in mesenchymal tissue, and Alcaligenes faecaiis was the dominant bacterium in the homogenate. In this treatment group neither chitinase nor cellulase activity was detected in the homogenates at any time during the experiment.

Alternaria sp.

Mites did not remain continually on the fungal cover; rather, they visited it for feeding, left it, and then returned. Observed parameters did not change throughout the length of the experiment, although grazing intensity gradually increased. Food boli consisted of a mixture of fungal cells; spores of Alicaligenes sp. were dominant, as were small, unidentified cells of bacterial nature. all boli were covered by a thick mucoid coat (Fig. 2b). As with the Protococcus group, secretory activity of the mesenteral caeca was strong and accompanied by dark cells. Feces were black even when inside the mites. Bacterial cells were rare in the mesenchymal tissue, and Alcaligenes faecaiis was the dominant bacterium in the homogenate. At no time was either chitinase or cellulase activity detected.

Filter paper

Mites visited the paper immediately with most remaining beneath it and some exploring the whole jar substrate. Grazing activity increased during the course of the experiment. After 10 days, the filter paper was covered by colonies of fungi, mostly of sterile mycelium.

On day 1, the alimentary tract was filled by mucus, with rare fragments of paper (Fig. 2c). After 3 days, fungal spores and fragments of hyphae appeared in boli (although no fungi were yet visually detected on paper), accompanied by an increased bacterial population in the mesenchymal tissue. secretory activity of the caeca was high and dark cells became very frequent in the caecal walls, as well as in the mesenchymal tissue between the internal organs. Chitinase activity was strong in the homogenate after 3 days, but cellulase was not detected. Alcaligenes faecaiis was the dominant bacterium in the homogenate throughout the experiment.

Figure 1. Archegozetes longisetosus, tritonymph, mesenteron and food boli on offered food (parasagittal sections): (a) Algal food, third day of consumption. Arrows point to fungal spores, arrowheads to algal cells, (b) Algal food, seventh day of consumption. Arrows point to fungal spores, arrowheads to algal cells, (c) Stachybothrys sp., third day of consumption, mesenteron with various types of fragments. Arrowheads point to proliferated apices of mesenteral cells, (d) Stachybothrys sp., detail of the fragments of paper (substrate of fungus) in mesenteron. Staining: Masson's trichrome.

Figure 2. Archegozetes tongisetosus, tritonymph, mesenteron and food boli on offered food (parasagittal sections): (a) Stachybothrys sp., seventh day of consumption. Arrowhead points to the mucoid coat on bolus, (b) Alternaria, food bolus consisting of fungal propagules, arrowhead points to the mucoid coat on bolus, arrowheads point to fungal spores, (c) filter paper, whole mite, (d) starvation, whole mite. Staining: Masson's trichrome. co colon, goap- genital papillae, me -mesenteron, mec mesenteral caecum, op- ovipositor, ov-ovarium.

Starvation (only plaster/charcoal bottom)

For the first 3 days, mites walked on the bottom of the jar, apparently haphazardly. They aggregated only on the dense accumulation of feces that resulted from ingested algae and invasive fungi in the original cultures.

On the first day, small food boli appeared irregularly in the alimentary tract, which otherwise was empty (Fig. 2d) or filled with mucus. Later, an increasing number of cells of bacterial nature and limited fungal propagules appeared, especially in the mesenteron, but these were not present in compact boli. Bacterial cells were rare in mesenchymal tissue in some specimens, but more frequent in others. In the homogenates, neither chitinase nor cellulase activity was detected, and the dominant bacteria were AkaUgenes sp. and Achromobacter xylosoxidans ssp. denitrificans.

Discussion

Information relating to the nutrition of Archegozetes longisetosus is slowly accumulating in the literature, but there is much inconsistency. Much of this information comes from Haq and colleagues who investigated the diet of a southern India population of A. longisetosus using field-collected specimens and laboratory investigations with naturally available potential foods. In one of these studies, Haq and Prabhoo (1977) found large amounts of fungal material but few leaf fragments in the guts of field-collected mites. Similar result-a high abundance of fungal hyphae and spores, a few algal cells, and no pollen, leaf or wood material-were later reported by Haq (1982), who considered the mite a microphytophage in the terminology of Luxton (1972). In a subsequent study, Haq (1996) found fungal material to be abundant in the guts of field-collected specimens, but leaf particles were even more so; he therefore considered A. longisetosus a panphytophagous (unspecialized) feeder.

Laboratory studies of this mite seem to have produced results that are surprisingly inconsistent. Haq and Prabhoo (1977) found that both adult and immature mites fed heavily on decaying leaves (contrasting to the field diet seen in the same study). Adults and immatures differed in their reaction to two common fungi: nymphs fed heavily on Alternaha sp. but rejected Thchoderma, while adults ate the latter to some degree but rejected the former. In contrast, Haq and Adolph (1981) found that nymphs ate both Trichoderma and Alternaria sp., but adults refused both. Haq (1982) reported similar results, except that both adults and immatures apparently rejected Trichoderma. Subsequently, Haq (1996) found that immatures fed on each of these fungi, but only casually. In this latter study A. longisetosus fed "intentionally" on only one of a long list of tested fungi (Coiletotrichum sp.) but this fungus was rejected in the earlier study of Haq and Prabhoo (1977).

The alga Protococcus has been used successfully as the primary food in many of the biological studies of A. longisetosus cited in the Material and Methods, above, but it was eaten only casually in the study of Haq (1996) and was entirely rejected in the earlier studies (Haq and Prabhoo, 1977; Haq, 1982). Brewery yeast is another food with inconsistent results. Haq (1996) found nymphs to feed on this substrate, but it was rejected in the studies of Haq and Prabhoo (1977) and Haq (1982). In contrast, Ms. B. Earner (personal communication, 2000) has maintained a subculture of the Puerto Rican mites on brewery yeast for long periods.

Since the parameters we studied reveal physical and chemical processes of digestion (cf. Smrz, 1996, 1998, 2001, 2002a,b), we can comment on high food utilization by distinguishing between the simple sucking of the food and its digestion. Chitinase (for most fungi) or cellulase (for algae) is necessary for full utilization, but not if only cell contents are used. The distribution and shape of food boli is also informative; the presence of compact boli with mucoid coats in all parts of the gut indicates high palatability and digestive activity. On the other hand, an empty digestive tract, or one with mucus or fragments irregularly distributed, indicates an unpalatable food. Mesenteral caeca secretion (apocrine pattern) also is correlated with active digestion. Furthermore, characteristics of the caecal walls differ depending on food. \On an algal diet the actively secreting walls of the caeca are translucent, with small dark granules. In contrast, fungal feeding results in the presence of dark cells (hemocytes) that penetrate the caecal walls. This, together with the chitinolytic bacteria (Serratia) inside the mite body (Smrz, 1996, 2001), corresponds to strong secretory activity (cf. Smrz, 2002a, b) and chitinase production.

Protococcus sp. proved a highly palatable and nutritious food for A. longisetosus, and was the only food that was totally consumed. This was not surprising, since these or similar green algae are readily eaten by some other oribatid mites (Sengbusch, 1963; Littlewood, 1969; Tarman, 1968), and algae were used as a food source in other biological studies of A. longisetosus, as mentioned above. However, the way in which algae were used was indeed surprising. Their digestion was clearly evident in the alimentary tract, but only simple substances seemed to be used, since no cellulase activity was noted. This is consistent with Tarman (1968) observation that cells of Pleurococcus passed through oribatid mite guts intact if they were not previously ruptured by feeding action. The incomplete or imperfect digestion of such palatable food within the gut seems peculiar, but it is congruent with the very slow digestion and passage of food through the alimentary tract, and also the low metabolic rate, that is generally associated with digestive processes of oribatid mites (Hoebel-Maevers, 1967; Luxton, 1972, 1981). Even though fungal propagules appeared in food boli during the later stages of grazing on algae (Figs. 1a and 2a), no chitinase was detected and we can assume that the fungal walls were not digested.

Stachybothrys is a reported food of several oribatid mites (e.g. Damaeus) as is Bothrytis, another cellulolytic fungus (see Smrz and Trelova, 1995; Smrz, 1996). However, A. /ong/setosus rejected Stachybothrys, even avoided it, and preferred to consume the filter paper substrate on which the fungus was grown. They may have been repelled by stachybothryotoxin, a compound produced by Stachybothrys that is toxic to both plants and animals (Mirchink, 1988). The change of food bolus structure after 5 days was probably due to ingestion of invasive microorganisms in the experimental jars.

Archegozetes /ong/sefosus grazed on Alternaria, despite its strong toxins (alternaric acid, patulin), which are lethal to many plants and animals (Mirchink, 1988). Tyrophagus putrescentiae, a common astigmatic soil mite, showed even greater tolerance of the toxins, as indicated by strong secretions in the caeca and rapid population increase on a diet of Alternaria (Smrz and Catska, 1987, 1989). This is consistent with the different reproductive biologies exhibited by these two soil mites (cf. Smrz and jungova, 1989).

Fungi can be utilized in ways that do not require digestion of the cell wall, such as crushing and swallowing of mycelium or spores, or sucking cell contents (Smrz and Catska, 1989). In both the Alternaria and Stachybothrys treatments, spores in the alimentary tract were nearly intact and seemed to have been swallowed whole.The absence of chitinase activity and chitinolytic bacteria in the gut of A. longisetosus on an Alternaria diet is consistent with such utilization, and suggests imperfect digestion and that probably only simple compounds are utilized. Thus, Alternaha sp. is a poor food for A. longisetosus, a conclusion that is generally consistent with the results of Haq (see above).

The digestive activity of A. longisetosus when provided only with filter paper was clearly influenced by the invasion of fungi after 3 days. These invasive fungi (most present as sterile mycelium, difficult or impossible to identify) seemed to be more palatable to mites than were Alternaria or Stachybothrys, as supported by several observations. After 10 days, chitinase activity in the homogenate was significant, and the fungal propagules in food boli appeared to be more damaged by crushing and digestion than earlier. Mites in this treatment also had the greatest development of bacterial groups in the mesenchymal tissue; the presence of such bacteria has been associated with chitinase activity in some soil saprophagous mites (Smrz, 1996, 2002a, b; Smrzetal., 1991). Also, the appearance of Serratia in homogenates seemed to correlate with chitinase activity, and is apparently induced by feeding on the palatable invading fungi.

A complete absence of food resulted in an empty mesenteron during the first 3 days. However, the mites "invested" the feces derived from previous food by re-ingesting some of this material directly and by consuming microorganisms that grew on them. The most common bacterium, Alcaligenes faecaUs, was also reported from Tyrop/iagus putrescentiae and other soil mites in some previous papers (Smrz and Catska, 1989; Smrz and Trelova, 1995; Smrzetal., 1991).

The range of palatability and digestive activity that we observed is consistent with the work of Seniczak (1998), who studied a separate subculture of the Puerto Rican population used in this study. She found that A. longisetosus could succeed eating only Cladonia lichen, or only the bark of Prunus padus L, but that development rate, size and fecundity were greatly diminished compared to individuals fed Protococcus algae.

The foods offered to Archegozetes /ong/seiosus during our experiment may not be important, or even available, in the mite's natural environment. However, our results show that diet can strongly influence the microanatomy and activity of the digestive tract of this mite, as well as the frequency and identity of internal bacteria. The idea that important enzymes are induced by the current diet is also supported and indicates that the characterization of the overall trophic level of a species by surveying instantaneous enzyme activity is potentially misleading.

That the diet and enzymatic activity of Archegozetes longisetosus and other oribatid mites can be plastic is also suggested by the fact that no notable mortality was recorded during the 10 days of our experiment, regardless of treatment. In each case, the experimental environment changed over time, either by total utilization of original food or by invasion of "wild" fungi. The mites are thus able to survive on various types of food (cf. Smrz, 1996, 2001, 2002a,b). Such grazing and digestive flexibility may partially explain inconsistencies in the literature regarding oribatid mite feeding biology. So, while the experimental results can indicate a range of possibilities, we must be careful in extrapolating complex natural environments.

Acknowledgements

This study was supported by grant 526/99/0681 from the Grant Agency of the Czech Republic GACR.

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Jaroslav Smrz(a),*, Roy A. Norton(b)

a Department of Zoology, Charles University, Vinicna 7 Praha 2, CZ-128 44 Czech Republic

b Department of Environmental and Forest Biology, College of Environmental Science and Forestry, State University of New York, Syracuse, NY 13210, USA

Received 5 August 2001; accepted 3 September 2003

* Corresponding author.

E-mail address: smrz@mbox.cesnet.cz (J. Smrz).

Copyright Urban & Fischer Verlag 2004

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